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Abstract

Ocean ecosystems are experiencing unprecedented rates of climate and anthropogenic change, which can often initiate stress in marine organisms. Symbioses, or associations between different organisms, are plentiful in the ocean and could play a significant role in facilitating organismal adaptations to stressful ocean conditions. This article reviews current knowledge about the role of symbiosis in marine organismal acclimation and adaptation. It discusses stress and adaptations in symbioses from coral reef ecosystems, which are among the most affected environments in the ocean, including the relationships between corals and microalgae, corals and bacteria, anemones and clownfish, and cleaner fish and client fish. Despite the importance of this subject, knowledge of how marine organisms adapt to stress is still limited, and there are vast opportunities for research and technological development in this area. Attention to this subject will enhance our understanding of the capacity of symbioses to alleviate organismal stress in the oceans.

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2020-01-03
2024-03-28
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Literature Cited

  1. Aanen DK, Eggleton P. 2017. Symbiogenesis: beyond the endosymbiosis theory. ? J. Theor. Biol. 434:99–103
    [Google Scholar]
  2. Ainsworth TD, Fine M, Roff G, Hoegh-Guldberg O 2007. Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica. . ISME J 2:67–73
    [Google Scholar]
  3. Ainsworth TD, Fordyce AJ, Camp EF 2017. The other microeukaryotes of the coral reef microbiome. Trends Microbiol 25:980–91
    [Google Scholar]
  4. Ainsworth TD, Gates RD. 2016. Corals’ microbial sentinels. Science 352:1518–19
    [Google Scholar]
  5. Apprill A, Marlow HQ, Martindale MQ, Rappé MS 2009. The onset of microbial association in the developing coral Pocillopora meandrina. . ISME J 3:685–99
    [Google Scholar]
  6. Apprill A, Weber L, Santoro A 2016. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems 1:e00143–16
    [Google Scholar]
  7. Arnal C, Verneau O, Desdevises Y 2006. Phylogenetic relationships and evolution of cleaning behaviour in the family Labridae: importance of body colour pattern. J. Evol. Biol. 19:755–63
    [Google Scholar]
  8. Baird AH, Bhagooli R, Ralph PJ, Takahashi S 2009. Coral bleaching: the role of the host. Trends Ecol. Evol. 24:16–20
    [Google Scholar]
  9. Baird AH, Marshall P. 1998. Mass bleaching of corals on the Great Barrier Reef. Coral Reefs 17:376
    [Google Scholar]
  10. Baker AC. 2001. Reef corals bleach to survive change. Nature 411:765–66
    [Google Scholar]
  11. Bay RA, Palumbi SR. 2014. Multilocus adaptation associated with heat resistance in reef-building corals. Curr. Biol. 24:2952–56
    [Google Scholar]
  12. Beldade R, Blandin A, O'Donnell R, Mills SC 2017. Cascading effects of thermally-induced anemone bleaching on associated anemonefish hormonal stress response and reproduction. Nat. Commun. 8:716
    [Google Scholar]
  13. Berkelmans R, van Oppen MJ 2006. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B 273:2305–12
    [Google Scholar]
  14. Bhagooli R, Hidaka M. 2004. Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar. Biol. 145:329–37
    [Google Scholar]
  15. Bîrluţiu RM, Bîrluţiu V, Cismasiu RS, Mihalache P, Mihalache M 2017. Bacterial biofilm: a mini-review of an emerging form of bacteria. Acta Med. Transilv. 22:68–71
    [Google Scholar]
  16. Bongrand C, Koch EJ, Moriano-Gutierrez S, Cordero OX, McFall-Ngai M et al. 2016. A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior. ISME J 10:2907
    [Google Scholar]
  17. Bongrand C, Ruby EG. 2019. Achieving a multi-strain symbiosis: strain behavior and infection dynamics. ISME J 13:698
    [Google Scholar]
  18. Boto L. 2014. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc. R. Soc. B 281:20132450
    [Google Scholar]
  19. Bourne DG, Morrow KM, Webster NS 2016. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70:317–40
    [Google Scholar]
  20. Brown BE. 1997. Coral bleaching: causes and consequences. Coral Reefs 16:S129–38
    [Google Scholar]
  21. Buddemeier RW, Fautin DG. 1993. Coral bleaching as an adaptive mechanism: a testable hypothesis. BioScience 43:320–26
    [Google Scholar]
  22. Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES et al. 2011. The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–55
    [Google Scholar]
  23. Buston PM, García M. 2007. An extraordinary life span estimate for the clown anemonefish Amphiprion percula. J. Fish Biol 70:1710–19
    [Google Scholar]
  24. Cao M, Goodrich-Blair H. 2017. Ready or not: microbial adaptive responses in dynamic symbiosis environments. J. Bacteriol. 199:e00883–16
    [Google Scholar]
  25. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–63
    [Google Scholar]
  26. Carrapiço F. 2010. How symbiogenic is evolution. ? Theory Biosci 129:135–39
    [Google Scholar]
  27. Cavalier-Smith T. 2013. Symbiogenesis: mechanisms, evolutionary consequences, and systematic implications. Annu. Rev. Ecol. Evol. Syst. 44:145–72
    [Google Scholar]
  28. Cheney KL, Grutter AS, Blomberg SP, Marshall NJ 2009. Blue and yellow signal cleaning behavior in coral reef fishes. Curr. Biol. 19:1283–87
    [Google Scholar]
  29. Chiarello M, Auguet J-C, Bettarel Y, Bouvier C, Claverie T et al. 2018. Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet. Microbiome 6:147
    [Google Scholar]
  30. Christie PJ, Gordon JE. 2014. The Agrobacterium Ti plasmids. Microbiol. Spectrum 2:6 https://doi.org/10.1128/microbiolspec.PLAS-0010-2013
    [Crossref] [Google Scholar]
  31. Ciais P, Sabine C, Bala G, Bopp L, Brovkin V et al. 2013. Carbon and other biogeochemical cycles. See IPCC 2013 465–570
  32. Costanza R. 1999. The ecological, economic, and social importance of the oceans. Ecol. Econ. 31:199–213
    [Google Scholar]
  33. Costello MJ, Coll M, Danovaro R, Halpin P, Ojaveer H, Miloslavich P 2010. A census of marine biodiversity knowledge, resources, and future challenges. PLOS ONE 5:e12110
    [Google Scholar]
  34. Côté IM. 2000. Evolution and ecology of cleaning symbioses in the sea. Oceanogr. Mar. Biol. 38:311–55
    [Google Scholar]
  35. Cowman PF, Bellwood DR, van Herwerden L 2009. Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs. Mol. Phylogenet. Evol. 52:621–31
    [Google Scholar]
  36. Cunning R, Silverstein RN, Baker AC 2018. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs 37:145–52
    [Google Scholar]
  37. Damjanovic K, Blackall LL, Webster NS, van Oppen MJ 2017. The contribution of microbial biotechnology to mitigating coral reef degradation. Microb. Biotechnol. 10:1236–43
    [Google Scholar]
  38. de Bary A. 1879. The Phenomenon of Symbiosis Strasbourg, Ger.: Karl J. Trübner
  39. DeCarlo TM, Cohen AL, Barkley HC, Cobban Q, Young C et al. 2015. Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43:7–10
    [Google Scholar]
  40. Dixon GB, Bay LK, Matz MV 2016. Evolutionary consequences of DNA methylation in a basal metazoan. Mol. Biol. Evol. 33:2285–93
    [Google Scholar]
  41. Dodge KL, Kukulya AL, Burke E, Baumgartner MF 2018. TurtleCam: a “smart” autonomous underwater vehicle for investigating behaviors and habitats of sea turtles. Front. Mar. Sci. 5:90
    [Google Scholar]
  42. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F et al. 2012. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4:11–37
    [Google Scholar]
  43. Douglas AE. 1994. Symbiotic Interactions Oxford, UK: Oxford Univ. Press
  44. Douglas AE. 2010. The Symbiotic Habit Princeton, NJ: Princeton Univ. Press
  45. Duar RM, Frese SA, Lin XB, Fernando SC, Burkey TE et al. 2017. Experimental evaluation of host adaptation of Lactobacillus reuteri to different vertebrate species. Appl. Environ. Microbiol. 83:e00132–17
    [Google Scholar]
  46. Duarte CM. 2000. Marine biodiversity and ecosystem services: an elusive link. J. Exp. Mar. Biol. Ecol. 250:117–31
    [Google Scholar]
  47. Duperron S. 2017. Microbial Symbiosis London: ISTE Press
  48. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586–608
    [Google Scholar]
  49. Fautin DG. 1992. Anemonefish recruitment: the roles of order and chance. Symbiosis 14:143–60
    [Google Scholar]
  50. Feder HM. 1966. Cleaning symbiosis in the marine environment. Symbiosis 1:327–80
    [Google Scholar]
  51. Gilbert SF, McDonald E, Boyle N, Buttino N, Gyi L et al. 2010. Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos. Trans. R. Soc. B 365:671–78
    [Google Scholar]
  52. Gingins S, Roche DG, Bshary R 2017. Mutualistic cleaner fish maintains high escape performance despite privileged relationship with predators. Proc. R. Soc. B 284:20162469
    [Google Scholar]
  53. Goldenfeld N, Woese C. 2007. Biology's next revolution. Nature 445:369
    [Google Scholar]
  54. Gray MW, Doolittle WF. 1982. Has the endosymbiont hypothesis been proven. ? Microbiol. Rev. 46:1–42
    [Google Scholar]
  55. Grube M, White JF Jr., Seckbach J 2010. Symbioses and stress. Symbioses and Stress: Joint Ventures in Biology J Seckbach, M Grube 21–36 Dordrecht, Neth.: Springer
    [Google Scholar]
  56. Grutter AS. 1997. Spatiotemporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. . Copeia 1997:346–55
    [Google Scholar]
  57. Grutter AS. 1999. Cleaner fish really do clean. Nature 398:672–73
    [Google Scholar]
  58. Grutter AS, Bshary R. 2003. Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc. R. Soc. B 270:S242–44
    [Google Scholar]
  59. Grutter AS, De Brauwer M, Bshary R, Cheney KL, Cribb TH et al. 2018. Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37:15–24
    [Google Scholar]
  60. Grutter AS, Murphy JM, Choat JH 2003. Cleaner fish drives local fish diversity on coral reefs. Curr. Biol. 13:64–67
    [Google Scholar]
  61. Guerrero R, Margulis L, Berlanga M 2013. Symbiogenesis: the holobiont as a unit of evolution. Int. Microbiol. 16:133–43
    [Google Scholar]
  62. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F et al. 2008. A global map of human impact on marine ecosystems. Science 319:948–52
    [Google Scholar]
  63. Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo I et al. 2007. Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:1172–95
    [Google Scholar]
  64. Hazen EL, Jorgensen S, Rykaczewski RR, Bograd SJ, Foley DG et al. 2013. Predicted habitat shifts of Pacific top predators in a changing climate. Nat. Clim. Change 3:234–38
    [Google Scholar]
  65. Hoffmeister M, Martin W. 2003. Interspecific evolution: microbial symbiosis, endosymbiosis and gene transfer. Environ. Microbiol. 5:641–49
    [Google Scholar]
  66. Holles S, Simpson SD, Radford AN, Berten L, Lecchini D 2013. Boat noise disrupts orientation behaviour in a coral reef fish. Mar. Ecol. Prog. Ser. 485:295–300
    [Google Scholar]
  67. Huggett M, Apprill A. 2019. Coral Microbiome Database: Integration of sequences reveals high diversity and specificity of coral-associated microbes. Environ. Microbiol. Rep. 11:372–85
    [Google Scholar]
  68. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT et al. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
    [Google Scholar]
  69. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD et al. 2017. Global warming and recurrent mass bleaching of corals. Nature 543:373–77
    [Google Scholar]
  70. IPCC (Intergov. Panel Clim. Change) 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Ed. TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen et al. Cambridge, UK: Cambridge Univ. Press
  71. Jackson DJ, Macis L, Reitner J, Wörheide G 2011. A horizontal gene transfer supported the evolution of an early metazoan biomineralization strategy. BMC Evol. Biol. 11:238
    [Google Scholar]
  72. Jackson JB. 1991. Adaptation and diversity of reef corals. BioScience 41:475–82
    [Google Scholar]
  73. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B 275:1359–65
    [Google Scholar]
  74. Kelman D. 2004. Antimicrobial activity of sponges and corals. Coral Health and Disease E Rosenberg, Y Loya 243–58 Berlin: Springer
    [Google Scholar]
  75. Kiers ET, West SA. 2015. Evolving new organisms via symbiosis. Science 348:392–94
    [Google Scholar]
  76. Knowlton N, Rohwer F. 2003. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am. Nat. 162:S51–62
    [Google Scholar]
  77. [Google Scholar]
  78. Kushmaro A, Loya Y, Fine M, Rosenberg E 1996. Bacterial infection and coral bleaching. Nature 380:396
    [Google Scholar]
  79. Kwong WK, del Campo J, Mathur V, Vermeij MJ, Keeling PJ 2019. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568:103–7
    [Google Scholar]
  80. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD et al. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:2570–80.e6
    [Google Scholar]
  81. Lesser MP. 2011. Coral bleaching: causes and mechanisms. Coral Reefs: An Ecosystem in Transition Z Dubinsky, N Stambler 405–19 Dordrecht, Neth.: Springer
    [Google Scholar]
  82. Lewin RA. 1981. Prochloron and the theory of symbiogenesis. Ann. N.Y. Acad. Sci. 361:325–29
    [Google Scholar]
  83. Limbaugh C. 1961. Cleaning symbiosis. Sci. Am. 205:42–49
    [Google Scholar]
  84. Litsios G, Salamin N. 2014. Hybridisation and diversification in the adaptive radiation of clownfishes. BMC Evol. Biol. 14:245
    [Google Scholar]
  85. Litsios G, Sims CA, Wüest RO, Pearman PB, Zimmermann NE, Salamin N 2012. Mutualism with sea anemones triggered the adaptive radiation of clownfishes. BMC Evol. Biol. 12:212
    [Google Scholar]
  86. Losey GS. 1972. The ecological importance of cleaning symbiosis. Copeia 1972:820–33
    [Google Scholar]
  87. Madeira C, Madeira D, Diniz MS, Cabral HN, Vinagre C 2017. Comparing biomarker responses during thermal acclimation: a lethal versus non-lethal approach in a tropical reef clownfish. Comp. Biochem. Physiol. A 204:104–12
    [Google Scholar]
  88. Margulis L. 1970. Origin of Eukaryotic Cells: Evidence and Research Implications for a Theory of the Origin and Evolution of Microbial, Plant and Animal Cells on the Precambrian Earth New Haven, CT: Yale Univ. Press
  89. Margulis L. 1991. Symbiogenesis and symbionticism. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis L Margulis, R Fester 1–14 Cambridge, MA: MIT Press
    [Google Scholar]
  90. Margulis L. 2010. Symbiogenesis. A new principle of evolution rediscovery of Boris Mikhaylovich Kozo-Polyansky (1890–1957). Paleontol. J. 44:1525–39
    [Google Scholar]
  91. Margulis L, Sagan D. 1997. Microcosmos: Four Billion Years of Microbial Evolution Berkeley: Univ. Calif. Press
  92. McDevitt-Irwin JM, Baum JK, Garren M, Vega Thurber RL 2017. Responses of coral-associated bacterial communities to local and global stressors. Front. Mar. Sci. 4:262
    [Google Scholar]
  93. McFall-Ngai MJ. 1999. Consequences of evolving with bacterial symbionts: insights from the squid-vibrio associations. Annu. Rev. Ecol. Syst. 30:235–56
    [Google Scholar]
  94. McFall-Ngai MJ, Heath-Heckman EA, Gillette AA, Peyer SM, Harvie EA 2012. The secret languages of coevolved symbioses: insights from the Euprymna scolopes–Vibrio fischeri symbiosis. Semin. Immunol. 24:3–8
    [Google Scholar]
  95. Mebs D. 2009. Chemical biology of the mutualistic relationships of sea anemones with fish and crustaceans. Toxicon 54:1071–74
    [Google Scholar]
  96. Mereschkowsky C. 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen [Theory of two types of plasma as the basis of symbiogenesis, a new study of the origin of organisms]. Biol. Cent. 30:278–88, 289–303, 321–47, 353–67
    [Google Scholar]
  97. Merilaita S, Kelley JL. 2018. Scary clowns: adaptive function of anemonefish coloration. J. Evol. Biol. 31:1558–71
    [Google Scholar]
  98. Messias JP, Paula JR, Grutter AS, Bshary R, Soares MC 2016. Dopamine disruption increases negotiation for cooperative interactions in a fish. Sci. Rep. 6:20817
    [Google Scholar]
  99. Mitchell A, Romano GH, Groisman B, Yona A, Dekel E et al. 2009. Adaptive prediction of environmental changes by microorganisms. Nature 460:220–24
    [Google Scholar]
  100. Miyagawa-Kohshima K, Odoriba S, Okabe D, Baba Y, Touma H et al. 2014. Embryonic learning of chemical cues via the parents’ host in anemonefish (Amphiprion ocellaris). J. Exp. Mar. Biol. Ecol. 457:160–72
    [Google Scholar]
  101. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B 2011. How many species are there on Earth and in the ocean. ? PLOS Biol 9:e1001127
    [Google Scholar]
  102. Moran NA. 2003. Tracing the evolution of gene loss in obligate bacterial symbionts. Curr. Opin. Microbiol. 6:512–18
    [Google Scholar]
  103. Morrow K, Muller E, Lesser M 2018. How does the coral microbiome cause, respond to, or modulate the bleaching process. ? In Coral Bleaching: Patterns, Processes, Causes and Consequences MJ van Oppen, JM Lough 153–88 Cham, Switz.: Springer. , 2nd ed..
    [Google Scholar]
  104. Munday PL, Pratchett MS, Dixson DL, Donelson JM, Endo GG et al. 2013. Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish. Mar. Biol. 160:2137–44
    [Google Scholar]
  105. Muscatine L, Cernichiari E. 1969. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 137:506–23
    [Google Scholar]
  106. Nielsen DA, Petrou K, Gates RD 2018. Coral bleaching from a single cell perspective. ISME J 12:1558–67
    [Google Scholar]
  107. Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sørensen C et al. 2012. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Change 2:201–4
    [Google Scholar]
  108. Norin T, Mills SC, Crespel A, Cortese D, Killen SS, Beldade R 2018. Anemone bleaching increases the metabolic demands of symbiont anemonefish. Proc. R. Soc. B 285:20180282
    [Google Scholar]
  109. Nyholm SV, McFall-Ngai MJ. 2004. The winnowing: establishing the squid–Vibrio symbiosis. Nat. Rev. Microbiol. 2:632–42
    [Google Scholar]
  110. Nyström M, Folke C, Moberg F 2000. Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15:413–17
    [Google Scholar]
  111. O'Brien PA, Webster NS, Miller DJ, Bourne DG 2019. Host-microbe coevolution: applying evidence from model systems to complex marine invertebrate holobionts. mBio 10:e02241–18
    [Google Scholar]
  112. Ollerton J, McCollin D, Fautin DG, Allen GR 2006. Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts. Proc. R. Soc. B 274:591–98
    [Google Scholar]
  113. Paula JR, Messias JP, Grutter AS, Bshary R, Soares MC 2015. The role of serotonin in the modulation of cooperative behavior. Behav. Ecol. 26:1005–12
    [Google Scholar]
  114. Peixoto RS, Rosado PM, Leite DCDA, Rosado AS, Bourne DG 2017. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8:341
    [Google Scholar]
  115. Pollock FJ, McMinds R, Smith S, Bourne DG, Willis BL et al. 2018. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9:4921
    [Google Scholar]
  116. Porcar M, Latorre A, Moya A 2013. What symbionts teach us about modularity. Front. Bioeng. Biotechnol. 1:14
    [Google Scholar]
  117. Potts GW. 1968. The ethology of Crenilabrus melanocercus, with notes on cleaning symbiosis. J. Mar. Biol. Assoc. UK 48:279–93
    [Google Scholar]
  118. Pozo MJ, Azcón-Aguilar C. 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10:393–98
    [Google Scholar]
  119. Putnam HM, Davidson JM, Gates RD 2016. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9:1165–78
    [Google Scholar]
  120. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:2068–73
    [Google Scholar]
  121. Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A et al. 2014. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–209
    [Google Scholar]
  122. Ritchie KB. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322:1–14
    [Google Scholar]
  123. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N 2001. Diversity of bacteria associated with the Caribbean coral Montastraea franksi. . Coral Reefs 20:85–95
    [Google Scholar]
  124. Rohwer F, Seguritan V, Azam F, Knowlton N 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1–10
    [Google Scholar]
  125. Roopin M, Henry RP, Chadwick NE 2008. Nutrient transfer in a marine mutualism: patterns of ammonia excretion by anemonefish and uptake by giant sea anemones. Mar. Biol. 154:547–56
    [Google Scholar]
  126. Rosado PM, Leite DC, Duarte GA, Chaloub RM, Jospin G et al. 2018. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J 13:921–36
    [Google Scholar]
  127. Rosenberg E, Falkovitz L. 2004. The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 58:143–59
    [Google Scholar]
  128. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I 2007. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5:355–62
    [Google Scholar]
  129. Rowan R, Powers DA. 1991. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–51
    [Google Scholar]
  130. Russell SL. 2019. Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses: a systematic review and meta-analysis. FEMS Microbiol. Lett. 366:fnz013
    [Google Scholar]
  131. Rypien KL, Ward JR, Azam JR 2010. Antagonistic interactions among coral-associated bacteria. Environ. Microbiol. 12:28–39
    [Google Scholar]
  132. Saenz-Agudelo P, Jones G, Thorrold S, Planes S 2011. Detrimental effects of host anemone bleaching on anemonefish populations. Coral Reefs 30:497–506
    [Google Scholar]
  133. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O 2008. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. PNAS 105:10444–49
    [Google Scholar]
  134. Scott A, Dixson DL. 2016. Reef fishes can recognize bleached habitat during settlement: sea anemone bleaching alters anemonefish host selection. Proc. R. Soc. B 283:20152694
    [Google Scholar]
  135. Sharp KH, Ritchie KB, Schupp PJ, Ritson-Williams R, Paul VJ 2010. Bacterial acquisition in juveniles of several broadcast spawning coral species. PLOS ONE 5:e10898
    [Google Scholar]
  136. Shnit-Orland M, Kushmaro A. 2009. Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol. Ecol. 67:371–80
    [Google Scholar]
  137. Shostak S. 1993. A symbiogenetic theory for the origins of cnidocysts in Cnidaria. Biosystems 29:49–58
    [Google Scholar]
  138. Simpson SD, Radford AN, Holles S, Ferarri MC, Chivers DP et al. 2016. Small-boat noise impacts natural settlement behavior of coral reef fish larvae. The Effects of Noise on Aquatic Life II A Popper, A Hawkins 1041–48 New York: Springer
    [Google Scholar]
  139. Skillings D. 2016. Holobionts and the ecology of organisms: multi-species communities or integrated individuals. ? Biol. Philos. 31:875–92
    [Google Scholar]
  140. Skomal GB, Hoyos‐Padilla EM, Kukulya A, Stokey R 2015. Subsurface observations of white shark Carcharodon carcharias predatory behaviour using an autonomous underwater vehicle. J. Fish Biol. 87:1293–312
    [Google Scholar]
  141. Soares MC, Bshary R, Cardoso SC, Côté IM, Oliveira RF 2012. Face your fears: cleaning gobies inspect predators despite being stressed by them. PLOS ONE 7:e39781
    [Google Scholar]
  142. Soares MC, Cardoso SC, Côté IM 2007. Client preferences by Caribbean cleaning gobies: food, safety or something else. ? Behav. Ecol. Sociobiol. 61:1015
    [Google Scholar]
  143. Soares MC, Oliveira RF, Ros AF, Grutter AS, Bshary R 2011. Tactile stimulation lowers stress in fish. Nat. Commun. 2:534
    [Google Scholar]
  144. Stambler N. 2010. Coral symbiosis under stress. Symbioses and Stress: Joint Ventures in Biology J Seckbach, M Grube 197–224 Dordrecht, Neth.: Springer
    [Google Scholar]
  145. Starcevic A, Akthar S, Dunlap WC, Shick MJ, Hranueli D et al. 2008. Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis, have microbial origins. PNAS 105:2533–37
    [Google Scholar]
  146. Sudakaran S, Kost C, Kaltenpoth M 2017. Symbiont acquisition and replacement as a source of ecological innovation. Trends Microbiol 25:375–90
    [Google Scholar]
  147. Sweet M, Croquer A, Bythell J 2011. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
    [Google Scholar]
  148. Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L et al. 2017. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7:627–36
    [Google Scholar]
  149. Trench RK. 1971. The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by zooxanthellae in vitro. Proc. R. Soc. B 177:237–50
    [Google Scholar]
  150. van Beneden P-J. 1873. Un mot sur la vie sociale des animaux inférieurs. Bull. Acad. R. Belg. 2:779–96
    [Google Scholar]
  151. van Oppen MJ, Bongaerts P, Frade P, Peplow LM, Boyd SE et al. 2018. Adaptation to reef habitats through selection on the coral animal and its associated microbiome. Mol. Ecol. 27:2956–71
    [Google Scholar]
  152. van Oppen MJ, Oliver JK, Putnam HM, Gates RD 2015. Building coral reef resilience through assisted evolution. PNAS 112:2307–13
    [Google Scholar]
  153. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA et al. 2009. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11:2148–63
    [Google Scholar]
  154. Wallin IE. 1927. Symbionticism and the Origin of Species Baltimore, MD: Williams & Wilkins
  155. Webster NS, Reusch TB. 2017. Microbial contributions to the persistence of coral reefs. ISME J 11:2167–74
    [Google Scholar]
  156. Weis VM. 2008. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211:3059–66
    [Google Scholar]
  157. Wisshak M, Schönberg CH, Form A, Freiwald A 2012. Ocean acidification accelerates reef bioerosion. PLOS ONE 7:e45124
    [Google Scholar]
  158. Yoerger D, Curran M, Fujii J, German C, Gomez-Ibanez D et al. 2018. Mesobot: an autonomous underwater vehicle for tracking and sampling midwater targets Paper presented at the IEEE OES Autonomous Underwater Vehicle Symposium Porto, Port.: Nov. 6–9
  159. Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R et al. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7:11833
    [Google Scholar]
  160. Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR 2017. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8:14213
    [Google Scholar]
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